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Corals Sonja a Schwartz1*, Ann F Budd2 and David B Carlon3 Schwartz et al. BMC Evolutionary Biology 2012, 12:123 http://www.biomedcentral.com/1471-2148/12/123 RESEARCH ARTICLE Open Access Molecules and fossils reveal punctuated diversification in Caribbean “faviid” corals Sonja A Schwartz1*, Ann F Budd2 and David B Carlon3 Abstract Background: Even with well-known sampling biases, the fossil record is key to understanding macro-evolutionary patterns. During the Miocene to Pleistocene in the Caribbean Sea, the fossil record of scleractinian corals shows a remarkable period of rapid diversification followed by massive extinction. Here we combine a time-calibrated molecular phylogeny based on three nuclear introns with an updated fossil stratigraphy to examine patterns of radiation and extinction in Caribbean corals within the traditional family Faviidae. Results: Concatenated phylogenetic analysis showed most species of Caribbean faviids were monophyletic, with the exception of two Manicina species. The time-calibrated tree revealed the stem group originated around the closure of the Tethys Sea (17.0 Ma), while the genus Manicina diversified during the Late Miocene (8.20 Ma), when increased sedimentation and productivity may have favored free-living, heterotrophic species. Reef and shallow water specialists, represented by Diploria and Favia, originate at the beginning of the Pliocene (5 – 6 Ma) as the Isthmus of Panama shoaled and regional productivity declined. Conclusions: Later origination of the stem group than predicted from the fossil record corroborates the hypothesis of morphological convergence in Diploria and Favia genera. Our data support the rapid evolution of morphological and life-history traits among faviid corals that can be linked to Mio-Pliocene environmental changes. Keywords: Scleractinia, Speciation, Adaptive radiation, Miocene, Pliocene, Coral reef Background historical information from both molecular and fossil Explaining rapid diversification and speciation remains a data. By examining systems that show recent speciation central challenge to evolutionary biology [1,2]. Much within monophyletic groups, ecological differentiation, work has focused on either understanding the ecology and a strong fossil record, we can begin to link past to and phylogenetic history of species-rich systems that present processes in the understanding of the evolution have recently diversified along ecological axes (e.g. adap- of diversity. tive radiations) [3], or looking for patterns of species The marine Caribbean fauna provides rare examples of change in the fossil record [4-8]. Taking the molecular diversification of monophyletic lineages within the con- phylogenetic/ecological approach alone, however, text of well-understood changes in biogeography, ocean- excludes information about extinct lineages that may ography, and climate. The isolation of Caribbean substantially bias our ability to identify cases of rapid di- populations from their Indo-Pacific counterparts started versification [9]. Conversely, relying on the fossil record ~15-17 Ma when the closure of the Tethys Sea cut off alone limits our ability to detect evolutionary relation- connections between the Mediterranean and Indo- ships between fossil taxa and some shifts in ecological Pacific [10]. Isolation was complete ~3.45 - 4.25 Ma function that may not be apparent from fossil character when the rise of the Isthmus of Panama severed all states. Ultimately, a more complete understanding of Caribbean connections to the Indo-Pacific [11]. The the processes that drive rapid diversification will require period leading up to closure of the isthmus during the late Miocene to late Pliocene was characterized by chan- * Correspondence: [email protected] ging global oceanographic circulation patterns, leading 1Department of Environmental Science, Policy & Management, University of to drastic environmental, ecological, and taxonomic California, Berkeley, CA 94720, USA shifts within the Caribbean basin. Not only did the Full list of author information is available at the end of the article © 2012 Schwartz et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Schwartz et al. BMC Evolutionary Biology 2012, 12:123 Page 2 of 10 http://www.biomedcentral.com/1471-2148/12/123 cessation of gene flow between the Pacific and Atlantic demands an independent assessment of trends apparent Oceans lead to widespread vicariant speciation across in the fossil record. the newly formed isthmus [12-14], but on the Caribbean To explore the tempo and mode of this evolutionary di- side, the accompanying geological and oceanographic versification, we unite a new multi-locus phylogeny of the changes caused an overall decrease in depth, primary Caribbean Faviidae with new stratigraphic compilations productivity and turbidity and an increase in salinity, from the fossil record. Our well-sampled phylogeny temperature, and local environmental heterogeneity allows Bayesian approaches to place these relationships [11,15]. Fossil records of many marine taxa during this into a temporal context by dating divergence times based period show elevated levels of taxonomic turnover on molecular data and fossil calibrations. We compare [11,16-21], suggesting that climatic and geological vari- our time-calibrated phylogeny to temporal patterns of ables drove elevated rates of cladogenesis and extinction. origination and extinction revealed by the Neogene fossil This taxonomic turnover is particularly striking in cor- record, and find remarkable congruence between data als of the family Faviidae, where an examination of the sets. The timing of events revealed by this analysis stratigraphic ranges shows that all extant species origi- strongly implicates paleoenvironmental changes as dri- nated nearly simultaneously during the Mio-Pliocene vers of diversification in scleractinian corals. [22]. Moreover, for faviids, this recent radiation has resulted in impressive diversification of ecological and Results life-history traits [23,24]. Modern species of Manicina Phylogenetic analysis of Caribbean “Faviidae” are representative of a free-living lifestyle adapted to We sequenced three single copy nuclear loci for six sediment-rich seagrass habitats that expanded during the ingroup and one outgroup Caribbean faviid species. A Miocene then contracted during the Plio-Pleistocene total of 48 unique alleles were identified for CaM (align- [15]. In contrast, species of the brain coral genus Diploria ment length = 507 bp), 38 alleles were identified for tend to be reef-builders, dominating shallow water reef MaSC-1 (alignment length = 490 bp), and 55 alleles were platforms in Pleistocene and modern times [25-28]. identified for Pax-C (alignment length = 418 bp) (Add- These two “sediment” and “reef” clades appear to share a itional file 1). Maximum likelihood and Bayesian analysis common ancestor and ecological diversification seems to of gene trees showed little support for structure above have occurred over a short period of geological time, sug- the species level with no conflict between trees at highly gesting it is tied to the contemporaneous increase in en- supported nodes (Additional file 2). The taxa Manicina vironmental heterogeneity [29]. Yet this punctuated areolata and M. mayori shared some alleles at all loci, diversification event is inferred from a fossil record, and unique alleles isolated from Diploria clivosa and D. which may be incomplete or contain uncertainties in dat- strigosa did not always form monophyletic groups. A ing and taxonomic relationships that may influence our total of 94 individuals with unique genotypes were suc- interpretation of past patterns. cessfully sequenced at all three loci and used for a conca- Molecular data combined with well sampled fossil tenated phylogenetic analysis. See Additional file 3 for records provide opportunities to test existing evolution- genotype data of all individuals in study. ary hypotheses and extend our understanding of both Bayesian and maximum likelihood trees had identical the tempo and mode of evolutionary diversification. In topologies at all major nodes with support values the Scleractinia, deep divergences between coral orders, (Bayesian/ML bootstrap) indicated in Figure 1. The suborders and families are increasingly well understood ingroup node was well supported (100/100) as well as [30-33]. Yet a recent series of phylogenies exploring rela- species nodes for C. natans (100/100), D. clivosa (100/100), tionships at the familial level and below have demon- D. labyrinthiformis (100/98), D. strigosa (100/98) and strated pervasive polyphyly and paraphyly at the generic F. fragum (100/100). Manicina mayori and Manicina level [34-39]. In addition, these studies have shown that areolata failed to form monophyletic groups, though between ocean basins, species group geographically ra- support was high at the genus node for Manicina (100/ ther than taxonomically [35,38,39]. In particular, Atlantic 94). The genus Diploria failed to form a monophyletic lineages of Faviidae and Mussidae appear to be more group. Diploria clivosa formed a clade with Manicina closely related to other Atlantic lineages than to conge- spp. and D. strigosa formed a clade with Favia fragum. ners or even confamilials in other ocean basins. This Support for these nodes, however,
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